Untargeted Metabolic Quantitative Trait Loci Analyses Reveal a Relationship between Primary Metabolism and Potato Tuber Quality1[W][OA]

Recent advances in -omics technologies such as transcriptomics, metabolomics, and proteomics along with genotypic profiling have permitted dissection of the genetics of complex traits represented by molecular phenotypes in nonmodel species. To identify the genetic factors underlying variation in primary metabolism in potato (Solanum tuberosum), we have profiled primary metabolite content in a diploid potato mapping population, derived from crosses between S. tuberosum and wild relatives, using gas chromatography-time of flight-mass spectrometry. In total, 139 polar metabolites were detected, of which we identified metabolite quantitative trait loci for approximately 72% of the detected compounds. In order to obtain an insight into the relationships between metabolic traits and classical phenotypic traits, we also analyzed statistical associations between them. The combined analysis of genetic information through quantitative trait locus coincidence and the application of statistical learning methods provide information on putative indicators associated with the alterations in metabolic networks that affect complex phenotypic traits.

[1]  D. Corsini,et al.  Differences in free and protein-bound tyrosine among potato genotypes and the relationship to internal blackspot resistance , 1992, American Potato Journal.

[2]  Alison M. Smith,et al.  Starch: its metabolism, evolution, and biotechnological modification in plants. , 2010, Annual review of plant biology.

[3]  J. Szopa,et al.  The metabolic profile of the 14-3-3 repressed transgenic potato tubers , 2001 .

[4]  Twan America,et al.  From QTL to candidate gene: Genetical genomics of simple and complex traits in potato using a pooling strategy , 2010, BMC Genomics.

[5]  C. Bachem,et al.  Data integration and network reconstruction with ~omics data using Random Forest regression in potato. , 2011, Analytica chimica acta.

[6]  J. Preiss,et al.  Mutants of Arabidopsis with altered regulation of starch degradation. , 1991, Plant physiology.

[7]  Nell I. Mondy,et al.  Effect of maturity and storage on ascorbic acid and tyrosine concentrations and enzymic discoloration of potatoes , 1993 .

[8]  J. Keurentjes.  Genetical metabolomics: closing in on phenotypes. , 2009, Current opinion in plant biology.

[9]  H. Davies.  METABOLOMICS: APPLICATIONS IN FUNCTIONAL BIODIVERSITY ANALYSIS IN POTATO , 2007 .

[10]  S. Zeeman,et al.  Changes in carbohydrate metabolism and assimilate export in starch‐excess mutants of Arabidopsis , 1999 .

[11]  Lieven Sterck,et al.  Genetical metabolomics of flavonoid biosynthesis in Populus: a case study. , 2006, The Plant journal : for cell and molecular biology.

[12]  C. Foyer,et al.  Co-ordination of leaf minor amino acid contents in crop species: significance and interpretation. , 2002, Journal of experimental botany.

[13]  L. Sweetlove,et al.  Application of metabolite profiling to the identification of traits in a population of tomato introgression lines. , 2004, Journal of experimental botany.

[14]  S. Hizukuri.  Studies on Starch Phosphate , 1970 .

[15]  F. Salamini,et al.  A genetic analysis of quantitative resistance to late blight in potato: towards marker-assisted selection , 1999, Molecular Breeding.

[16]  U. Roessner,et al.  Technical advance: simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. , 2000, The Plant journal : for cell and molecular biology.

[17]  W. Stiekema,et al.  Multiple alleles for tuber shape in diploid potato detected by qualitative and quantitative genetic analysis using RFLPs. , 1994, Genetics.

[18]  Bjarne Gram Hansen,et al.  Biochemical Networks and Epistasis Shape the Arabidopsis thaliana Metabolome[W] , 2008, The Plant Cell Online.

[19]  J. Jacobsen,et al.  Application of molecular markers in the genetic analysis of quantitative traits. , 1996 .

[20]  Leo Breiman,et al.  Random Forests , 2001, Machine Learning.

[21]  C. Gebhardt,et al.  Tagging quantitative trait loci for maturity-corrected late blight resistance in tetraploid potato with PCR-based candidate gene markers. , 2004, Molecular plant-microbe interactions : MPMI.

[22]  Chi-Tang Ho,et al.  Enhancement of the primary flavor compound methional in potato by increasing the level of soluble methionine. , 2003, Journal of agricultural and food chemistry.

[23]  Jingyuan Fu,et al.  The genetics of plant metabolism , 2006, Nature Genetics.

[24]  M. Steup,et al.  The starch-related R1 protein is an alpha -glucan, water dikinase. , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[25]  J. Nap,et al.  Genetical genomics : the added value from segregation , 2001 .

[26]  A. Blennow,et al.  Functional characterization of alpha-glucan,water dikinase, the starch phosphorylating enzyme. , 2004, The Biochemical journal.

[27]  J. Ashurst,et al.  Pantothenate biosynthesis in higher plants: advances and challenges , 2006 .

[28]  Z. Bánfalvi,et al.  The effects of enhanced methionine synthesis on amino acid and anthocyanin content of potato tubers , 2008, BMC Plant Biology.

[29]  A. Fernie,et al.  Gas chromatography mass spectrometry–based metabolite profiling in plants , 2006, Nature Protocols.

[30]  M. Paul,et al.  Highly conserved protein kinases involved in the regulation of carbon and amino acid metabolism. , 2003, Journal of experimental botany.

[31]  Richard G. F. Visser,et al.  Unravelling enzymatic discoloration in potato through a combined approach of candidate genes, QTL, and expression analysis , 2007, Theoretical and Applied Genetics.

[32]  R. Doerge.  Multifactorial genetics: Mapping and analysis of quantitative trait loci in experimental populations , 2002, Nature Reviews Genetics.

[33]  P. Bliss,et al.  Identification of loci affecting flavour volatile emissions in tomato fruits. , 2006, Journal of experimental botany.

[34]  F. Carrari,et al.  Modulation of fructokinase activity of potato (Solanum tuberosum) results in substantial shifts in tuber metabolism. , 2005, Plant & cell physiology.

[35]  R. Waugh,et al.  QTL for field resistance to late blight in potato are strongly correlated with maturity and vigour , 2004, Molecular Breeding.

[36]  O. Fiehn,et al.  Process for the integrated extraction, identification and quantification of metabolites, proteins and RNA to reveal their co‐regulation in biochemical networks , 2004, Proteomics.

[37]  A. Weber,et al.  The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter. , 2001, The Plant cell.

[38]  Joost T. van Dongen,et al.  Discovering plant metabolic biomarkers for phenotype prediction using an untargeted approach. , 2010, Plant biotechnology journal.

[39]  D. Wiesenborn,et al.  Potato Starch Paste Behavior as Related to Some Physical/Chemical Properties , 1994 .

[40]  Y. M. Tikunov,et al.  MSClust: a tool for unsupervised mass spectra extraction of chromatography-mass spectrometry ion-wise aligned data , 2011, Metabolomics.

[41]  U. Roessner,et al.  Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement , 2006, Nature Biotechnology.

[42]  Arjen Lommen,et al.  MetAlign: interface-driven, versatile metabolomics tool for hyphenated full-scan mass spectrometry data preprocessing. , 2009, Analytical chemistry.

[43]  Alison M. Smith,et al.  Starch degradation. , 2005, Annual Review of Plant Biology.

[44]  Joachim Selbig,et al.  The metabolic signature related to high plant growth rate in Arabidopsis thaliana , 2007, Proceedings of the National Academy of Sciences.

[45]  Richard G. F. Visser,et al.  Identification of alleles of carotenoid pathway genes important for zeaxanthin accumulation in potato tubers , 2010, Plant Molecular Biology.

[46]  Joachim Selbig,et al.  Identification of metabolic and biomass QTL in Arabidopsis thaliana in a parallel analysis of RIL and IL populations , 2007, The Plant journal : for cell and molecular biology.

[47]  Yury Tikunov,et al.  A Novel Approach for Nontargeted Data Analysis for Metabolomics. Large-Scale Profiling of Tomato Fruit Volatiles1[w] , 2005, Plant Physiology.

[48]  Jan Hummel,et al.  Retention index thresholds for compound matching in GC-MS metabolite profiling. , 2008, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[49]  Ute Roessner,et al.  Simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. , 2000 .

[50]  A. Fernie,et al.  Metabolomics-assisted breeding: a viable option for crop improvement? , 2009, Trends in genetics : TIG.

[51]  Alisdair R. Fernie,et al.  Profiling of diurnal patterns of metabolite and transcript abundance in potato (Solanum tuberosum) leaves , 2005, Planta.

[52]  Derek Stewart,et al.  A metabolomics study of cultivated potato (Solanum tuberosum) groups Andigena, Phureja, Stenotomum, and tuberosum using gas chromatography-mass spectrometry. , 2010, Journal of agricultural and food chemistry.

[53]  Derek Stewart,et al.  Phytochemical diversity in tubers of potato cultivars and landraces using a GC-MS metabolomics approach. , 2008, Journal of agricultural and food chemistry.

[54]  R. Yada,et al.  Effect of Low Temperature Storage on Sugar Concentrations and Chip Color of Certain Processing Potato Cultivars and Selections , 1987 .

[55]  B. C. Celis-Gamboa.  The life cycle of the potato (Solanum tuberosum L.) : from crop physiology to genetics , 2002 .

[56]  S. Tabata,et al.  Studies on Starch Phosphate Part 1. Estimation of glucose-6-phosphate residues in starch and the presence of other bound phosphate(s) , 1970 .

[57]  A. Blennow,et al.  Structural, physicochemical, and pasting properties of starches from potato plants with repressed r1-gene. , 2001, Biomacromolecules.

[58]  H. Kleinkauf.  The role of 4'-phosphopantetheine in t' biosynthesis of fatty acids, polyketides and peptides. , 2000, BioFactors.

[59]  David M. A. Martin,et al.  Genome sequence and analysis of the tuber crop potato , 2011, Nature.

[60]  M. Tsuhako,et al.  The Reaction of cyclo-Triphosphate with L-α- or β-Alanine , 1985 .

[61]  Jingyuan Fu,et al.  MetaNetwork: a computational protocol for the genetic study of metabolic networks , 2007, Nature Protocols.

[62]  L. H. Lampitt,et al.  The phosphorus compounds of wheat starch. , 1949, The Biochemical journal.

[63]  L. Willmitzer,et al.  Inhibition of a starch-granule–bound protein leads to modified starch and repression of cold sweetening , 1998, Nature Biotechnology.

[64]  M. Steup,et al.  The starch-related R1 protein is an α-glucan, water dikinase , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[65]  D. Zamir,et al.  A genetic map of candidate genes and QTLs involved in tomato fruit size and composition. , 2004, Journal of experimental botany.